Defaunation leads to interaction deficits, not interaction compensation, in an island seed dispersal network.

Following defaunation, the loss of interactions with mutualists such as pollinators or seed dispersers may be compensated through increased interactions with remaining mutualists, ameliorating the negative cascading impacts on biodiversity. Alternatively, remaining mutualists may respond to altered competition by reducing the breadth or intensity of their interactions, exacerbating negative impacts on biodiversity. Despite the importance of these responses for our understanding of the dynamics of mutualistic networks and their response to global change, the mechanism and magnitude of interaction compensation within real mutualistic networks remains largely unknown. We examined differences in mutualistic interactions between frugivores and fruiting plants in two island ecosystems possessing an intact or disrupted seed dispersal network. We determined how changes in the abundance and behavior of remaining seed dispersers either increased mutualistic interactions (contributing to "interaction compensation") or decreased interactions (causing an "interaction deficit") in the disrupted network. We found a "rich-get-richer" response in the disrupted network, where remaining frugivores favored the plant species with highest interaction frequency, a dynamic that worsened the interaction deficit among plant species with low interaction frequency. Only one of five plant species experienced compensation and the other four had significant interaction deficits, with interaction frequencies 56-95% lower in the disrupted network. These results do not provide support for the strong compensating mechanisms assumed in theoretical network models, suggesting that existing network models underestimate the prevalence of cascading mutualism disruption after defaunation. This work supports a mutualist biodiversity-ecosystem functioning relationship, highlighting the importance of mutualist diversity for sustaining diverse and resilient ecosystems.

Mutualistic strategies minimize coextinction in plant-disperser networks.

The global decline of mutualists such as pollinators and seed dispersers may cause negative direct and indirect impacts on biodiversity. Mutualistic network models used to understand the stability of mutualistic systems indicate that species with low partner diversity are most vulnerable to coextinction following mutualism disruption. However, existing models have not considered how species vary in their dependence on mutualistic interactions for reproduction or survival, overlooking the potential influence of this variation on species' coextinction vulnerability and on network stability. Using global databases and field experiments focused on the seed dispersal mutualism, we found that plants and animals that depend heavily on mutualistic interactions have higher partner diversity. Under simulated network disruption, this empirical relationship strongly reduced coextinction because the species most likely to lose mutualists depend least on their mutualists. The pattern also reduced the importance of network structure for stability; nested network structure had little effect on coextinction after simulations incorporated the empirically derived relationship between partner diversity and mutualistic dependence. Our results highlight a previously unknown source of stability in mutualistic networks and suggest that differences among species in their mutualistic strategy, rather than network structure, primarily accounts for stability in mutualistic communities.

How fragmentation and corridors affect wind dynamics and seed dispersal in open habitats.

Determining how widespread human-induced changes such as habitat loss, landscape fragmentation, and climate instability affect populations, communities, and ecosystems is one of the most pressing environmental challenges. Critical to this challenge is understanding how these changes are affecting the movement abilities and dispersal trajectories of organisms and what role conservation planning can play in promoting movement among remaining fragments of suitable habitat. Whereas evidence is mounting for how conservation strategies such as corridors impact animal movement, virtually nothing is known for species dispersed by wind, which are often mistakenly assumed to not be limited by dispersal. Here, we combine mechanistic dispersal models, wind measurements, and seed releases in a large-scale experimental landscape to show that habitat corridors affect wind dynamics and seed dispersal by redirecting and bellowing airflow and by increasing the likelihood of seed uplift. Wind direction interacts with landscape orientation to determine when corridors provide connectivity. Our results predict positive impacts of connectivity and patch shape on species richness of wind-dispersed plants, which we empirically illustrate using 12 y of data from our experimental landscapes. We conclude that habitat fragmentation and corridors strongly impact the movement of wind-dispersed species, which has community-level consequences.

Disentangling fragmentation effects on herbivory in understory plants of longleaf pine savanna.

Habitat fragmentation affects species and their interactions through intertwined mechanisms that include changes to fragment area, shape, connectivity and distance to edge. Disentangling these pathways is a fundamental challenge of landscape ecology and will help identify ecological processes important for management of rare species or restoration of fragmented habitats. In a landscape experiment that manipulated connectivity, fragment shape, and distance to edge while holding fragment area constant, we examined how fragmentation impacts herbivory and growth of nine plant species in longleaf pine savanna. Probability of herbivory in open habitat was strongly dependent on proximity to forest edge for every species, increasing with distance to edge in six species (primarily grasses and annual forbs) and decreasing in three species (perennial forbs and a shrub). In the two species of perennial forbs, these edge effects were dependent on fragment shape; herbivory strongly decreased with distance to edge in fragments of two shapes, but not in a third shape. For most species, however, probability of herbivory was unrelated to connectivity or fragment shape. Growth was generally determined more strongly by leaf herbivory than by distance to edge, fragment shape, or connectivity. Taken together, these results demonstrate consistently strong edge effects on herbivory, one of the most important biotic factors determining plant growth and demography. Our results contrast with the generally inconsistent results of observational studies, likely because our experimental approach enabled us to tease apart landscape processes that are typically confounded.

Connectivity from a different perspective: comparing seed dispersal kernels in connected vs. unfragmented landscapes.

Habitat fragmentation can create significant impediments to dispersal. A technique to increase dispersal between otherwise isolated fragments is the use of corridors. Although previous studies have compared dispersal between connected fragments to dispersal between unconnected fragments, it remains unknown how dispersal between fragments connected by a corridor compares to dispersal in unfragmented landscapes. To assess the extent to which corridors can restore dispersal in fragmented landscapes to levels observed in unfragmented landscapes, we employed a stable-isotope marking technique to track seeds within four unfragmented landscapes and eight experimental landscapes with fragments connected by corridors. We studied two wind- and two bird-dispersed plant species, because previous community-based research showed that dispersal mode explains how connectivity effects vary among species. We constructed dispersal kernels for these species in unfragmented landscapes and connected fragments by marking seeds in the center of each landscape with 'IN and then recovering marked seeds in seed traps at distances up to 200 m. For the two wind-dispersed plants, seed dispersal kernels were similar in unfragmented landscapes and connected fragments. In contrast, dispersal kernels of bird-dispersed seeds were both affected by fragmentation and differed in the direction of the impact: Morella cerifera experienced more and Rhus copallina experienced less long-distance dispersal in unfragmented than in connected landscapes. These results show that corridors can facilitate dispersal probabilities comparable to those observed in unfragmented landscapes. Although dispersal mode may provide useful broad predictions, we acknowledge that similar species may respond uniquely due to factors such as seasonality and disperser behavior. Our results further indicate that prior work has likely underestimated dispersal distances of wind-dispersed plants and that factors altering long-distance dispersal may have a greater impact on the spread of species than previously thought.

Gut passage and secondary metabolites alter the source of post-dispersal predation for bird-dispersed chili seeds.

Plants can influence the source and severity of seed predation through various mechanisms; the use of secondary metabolites for chemical defense, for example, is well documented. Gut passage by frugivores can also reduce mortality of animal-dispersed seeds, although this mechanism has gained far less attention than secondary metabolites. Apart from influencing the severity of seed predation, gut passage may also influence the source of seed predation. In Bolivia, we compared impacts of these two mechanisms, gut passage and secondary metabolites, on the source of seed predation in Capsicum chacoense, a wild chili species that is polymorphic for pungency (individual plants either produce fruits and seeds containing or lacking capsaicinoids). Using physical exclosures, we isolated seed removal by insects, mammals, and birds; seeds in the trials were from either pungent or non-pungent fruits and were either passed or not passed by seed-dispersing birds. Pungency had little influence on total short-term seed removal by animals, although prior work on this species indicates that capsaicin reduces mortality caused by fungi at longer time scales. Gut passage strongly reduced removal by insects, altering the relative impact of the three predator types. The weak impact of pungency on short-term predation contrasts with previous studies, highlighting the context dependence of secondary metabolites. The strong impact of gut passage demonstrates that this mechanism alone can influence which seed predators consume seeds, and that impacts of gut passage can be larger than those of secondary metabolites, which are more commonly acknowledged as a defense mechanism.

The influence of habitat fragmentation on multiple plant-animal interactions and plant reproduction.

Despite broad recognition that habitat loss represents the greatest threat to the world's biodiyersity, a mechanistic understanding of how habitat loss and associated fragmentation affect ecological systems has proven remarkably challenging. The challenge stems from the multiple interdependent ways that landscapes change following fragmentation and the ensuing complex impacts on populations and communities of interacting species. We confronted these challenges by evaluating how fragmentation affects individual plants through interactions with animals, across five herbaceous species native to longleaf pine savannas. We created a replicated landscape experiment that provides controlled tests of three major fragmentation effects (patch isolation, patch shape [i.e., edge-to-area ratio], and distance to edge), established experimental founder populations of the five species to control for spatial distributions and densities of individual plants, and employed structural equation modeling to evaluate the effects of fragmentation on plant reproductive output and the degree to which these impacts are mediated through altered herbivory, pollination, or pre-dispersal seed predation. Across species, the most consistent response to fragmentation was a reduction in herbivory. Herbivory, however, had little impact.on plant reproductive output, and thus we found little evidence for any resulting benefit to plants in fragments. In contrast, fragmentation rarely impacted pollination or pre-dispersal seed predation, but both of these interactions had strong and consistent impacts on plant reproductive output. As a result, our models robustly predicted plant reproductive output (r2 = 0.52-0.70), yet due to the weak effects of fragmentation on pollination and pre-dispersal seed predation, coupled with the weak effect of herbivory on plant reproduction, the effects of fragmentation on reproductive output were generally small in magnitude and inconsistent. This work provides mechanistic insight into landscape-scale variation in plant reproductive success, the relative importance of plant-animal interactions for structuring these dynamics, and the nuanced nature of how habitat fragmentation can affect populations and communities of interacting species.

Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition.

Specialised natural enemies maintain forest diversity by reducing tree survival in a density- or distance-dependent manner. Fungal pathogens, insects and mammals are the enemy types most commonly hypothesised to cause this phenomenon. Still, their relative importance remains largely unknown, as robust manipulative experiments have generally targeted a single enemy type and life history stage. Here, we use fungicide, insecticide and physical exclosure treatments to isolate the impacts of each enemy type on two life history stages (germination and early seedling survival) in three tropical tree species. Distance dependence was evident for five of six species-stage combinations, with each enemy type causing distance dependence for at least one species stage and their importance varying widely between species and stages. Rather than implicating one enemy type as the primary agent of this phenomenon, our field experiments suggest that multiple agents acting at different life stages collectively contribute to this diversity-promoting mechanism.

The impact of seasonality in temperature on thermal tolerance and elevational range size.

Environmental temperature variation can influence physiology, biogeography, and life history, with large consequences for ecology, evolution, and the impacts of climate change. Based on the seasonality hypothesis, greater annual temperature variation at high latitudes should result in greater thermal tolerance and, consequently, larger elevational ranges in temperate compared to tropical species. Despite the mechanistic nature of this hypothesis, most research has used latitude as a proxy for seasonality, failing to directly examine the impact of temperature variation on physiology and range size. We used phylogenetically matched beetles from locations spanning 60 degrees of latitude to explore links between seasonality, physiology and elevational range. Thermal tolerance increased with seasonality across all beetle groups, but realized seasonality (temperature variation restricted to the months species are active) was a better predictor of thermal tolerance than was annual seasonality. Additionally, beetles with greater thermal tolerance had larger elevational ranges. Our results support a mechanistic framework linking variation in realized temperature to physiology and distributions.

Landscape corridors can increase invasion by an exotic species and reduce diversity of native species.

Landscape corridors are commonly used to mitigate negative effects of habitat fragmentation, but concerns persist that they may facilitate the spread of invasive species. In a replicated landscape experiment of open habitat, we measured effects of corridors on the invasive fire ant, Solenopsis invicta, and native ants. Fire ants have two social forms: polygyne, which tend to disperse poorly but establish at high densities, and monogyne, which disperse widely but establish at lower densities. In landscapes dominated by polygyne fire ants, fire ant abundance was higher and native ant diversity was lower in habitat patches connected by corridors than in unconnected patches. Conversely, in landscapes dominated by monogyne fire ants, connectivity had no influence on fire ant abundance and native ant diversity. Polygyne fire ants dominated recently created landscapes, suggesting that these corridor effects may be transient. Our results suggest that corridors can facilitate invasion and they highlight the importance of considering species' traits when assessing corridor utility.

When condition trumps location: seed consumption by fruit-eating birds removes pathogens and predator attractants.

Seed ingestion by frugivorous vertebrates commonly benefits plants by moving seeds to locations with fewer predators and pathogens than under the parent. For plants with high local population densities, however, movement from the parent plant is unlikely to result in 'escape' from predators and pathogens. Changes to seed condition caused by gut passage may also provide benefits, yet are rarely evaluated as an alternative. Here, we use a common bird-dispersed chilli pepper (Capsicum chacoense) to conduct the first experimental comparison of escape-related benefits to condition-related benefits of animal-mediated seed dispersal. Within chilli populations, seeds dispersed far from parent plants gained no advantage from escape alone, but seed consumption by birds increased seed survival by 370% - regardless of dispersal distance - due to removal during gut passage of fungal pathogens and chemical attractants to granivores. These results call into question the pre-eminence of escape as the primary advantage of dispersal within populations and document two overlooked mechanisms by which frugivores can benefit fruiting plants.

Can terrestrial ectotherms escape the heat of climate change by moving?

Whether movement will enable organisms to alleviate thermal stress is central to the biodiversity implications of climate change. We use the temperature-dependence of ectotherm performance to investigate the fitness consequences of movement. Movement to an optimal location within a 50 km radius will only offset the fitness impacts of climate change by 2100 in 5 per cent of locations globally. Random movement carries an 87 per cent risk of further fitness detriment. Mountainous regions with high temperature seasonality (i.e. temperate areas) not only offer the greatest benefit from optimal movement but also the most severe fitness consequences if an organism moves to the wrong location. Doubling dispersal capacity would provide modest benefit exclusively to directed dispersers in topographically diverse areas. The benefits of movement for escaping climate change are particularly limited in the tropics, where fitness impacts will be most severe. The potential of movement to lessen climate change impacts may have been overestimated.

Connectivity planning to address climate change.

As the climate changes, human land use may impede species from tracking areas with suitable climates. Maintaining connectivity between areas of different temperatures could allow organisms to move along temperature gradients and allow species to continue to occupy the same temperature space as the climate warms. We used a coarse-filter approach to identify broad corridors for movement between areas where human influence is low while simultaneously routing the corridors along present-day spatial gradients of temperature. We modified a cost-distance algorithm to model these corridors and tested the model with data on current land-use and climate patterns in the Pacific Northwest of the United States. The resulting maps identified a network of patches and corridors across which species may move as climates change. The corridors are likely to be robust to uncertainty in the magnitude and direction of future climate change because they are derived from gradients and land-use patterns. The assumptions we applied in our model simplified the stability of temperature gradients and species responses to climate change and land use, but the model is flexible enough to be tailored to specific regions by incorporating other climate variables or movement costs. When used at appropriate resolutions, our approach may be of value to local, regional, and continental conservation initiatives seeking to promote species movements in a changing climate. Planificación de Conectividad para Atender el Cambio Climático.

Why are not all chilies hot? A trade-off limits pungency.

Evolutionary biologists increasingly recognize that evolution can be constrained by trade-offs, yet our understanding of how and when such constraints are manifested and whether they restrict adaptive divergence in populations remains limited. Here, we show that spatial heterogeneity in moisture maintains a polymorphism for pungency (heat) among natural populations of wild chilies (Capsicum chacoense) because traits influencing water-use efficiency are functionally integrated with traits controlling pungency (the production of capsaicinoids). Pungent and non-pungent chilies occur along a cline in moisture that spans their native range in Bolivia, and the proportion of pungent plants in populations increases with greater moisture availability. In high moisture environments, pungency is beneficial because capsaicinoids protect the fruit from pathogenic fungi, and is not costly because pungent and non-pungent chilies grown in well-watered conditions produce equal numbers of seeds. In low moisture environments, pungency is less beneficial as the risk of fungal infection is lower, and carries a significant cost because, under drought stress, seed production in pungent chilies is reduced by 50 per cent relative to non-pungent plants grown in identical conditions. This large difference in seed production under water-stressed (WS) conditions explains the existence of populations dominated by non-pungent plants, and appears to result from a genetic correlation between pungency and stomatal density: non-pungent plants, segregating from intra-population crosses, exhibit significantly lower stomatal density (p = 0.003), thereby reducing gas exchange under WS conditions. These results demonstrate the importance of trait integration in constraining adaptive divergence among populations.

Habitat patch shape, not corridors, determines herbivory and fruit production of an annual plant.

Habitat corridors confer many conservation benefits by increasing movement of organisms between habitat patches, but the benefits for some species may exact costs for others. For example, corridors may increase the abundance of consumers in a habitat to the detriment of the species they consume. In this study we assessed the impact of corridors on insect herbivory of a native plant, Solanum americanum, in large-scale, experimentally fragmented landscapes. We quantified leaf herbivory and assessed fruit production as a proxy for plant fitness. We also conducted field surveys of grasshoppers (Orthoptera), a group of abundant, generalist herbivores that feed on S. americanum, and we used exclosure cages to explicitly link grasshopper herbivory to fruit production of individual S. americanum. The presence of corridors did not increase herbivory or decrease plant fruit production. Likewise, corridors did not increase grasshopper abundance. Instead, patches in our landscapes with the least amount of edge habitat and the greatest amount of warmer "core" area had the highest levels of herbivory, the largest cost to plant fruit production as a result of herbivory, and the most grasshoppers. Thus habitat quality, governed by patch shape, can be more important than connectivity for determining levels of herbivory and the impact of herbivory on plant fitness in fragmented landscapes.

Landscape connectivity promotes plant biodiversity spillover into non-target habitats.

Conservation efforts typically focus on maximizing biodiversity in protected areas. The space available for reserves is limited, however, and conservation efforts must increasingly consider how management of protected areas can promote biodiversity beyond reserve borders. Habitat corridors are considered an important feature of reserves because they facilitate movement of organisms between patches, thereby increasing species richness in those patches. Here we demonstrate that by increasing species richness inside target patches, corridors additionally benefit biodiversity in surrounding non-target habitat, a biodiversity "spillover" effect. Working in the world's largest corridor experiment, we show that increased richness extends for approximately 30% of the width of the 1-ha connected patches, resulting in 10-18% more vascular plant species around patches of target habitat connected by corridors than around unconnected but otherwise equivalent patches of habitat. Furthermore, corridor-enhanced spillover into non-target habitat can be predicted by a simple plant life-history trait: seed dispersal mode. Species richness of animal-dispersed plants in non-target habitat increased in response to connectivity provided by corridors, whereas species richness of wind-dispersed plants was unaffected by connectivity and increased in response to changes in patch shape--higher edge-to-interior ratio--created by corridors. Corridors promoted biodiversity spillover for native species of the threatened longleaf pine ecosystem being restored in our experiment, but not for exotic species. By extending economically driven spillover concepts from marine fisheries and crop pollination systems, we show how reconnecting landscapes amplifies biodiversity conservation both within and beyond reserve borders.

Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure.

Both tropical and temperate species are responding to global warming through range shifts, but our understanding of the consequences of these shifts for whole communities is limited. Here, we use current elevational range data for six taxonomic groups spanning 90° in latitude to examine the potential impacts of climate-driven range shifts on community change, or 'disassembly', across latitude. Elevational ranges are smaller at low latitudes for most groups and, as a consequence, tropical communities appear to be more sensitive to temperature increases compared with temperate communities. Under site-specific temperature projections, we generally found greater community disassembly in tropical compared with temperate communities, although this varied by dispersal assumptions. Mountain height can impact the amount of community disassembly, with greater change occurring on smaller mountains. Finally, projected community disassembly was higher for ectotherms than endotherms, although the variation among ectotherms was greater than the variation separating endotherms and ectotherms.

The movement ecology and dynamics of plant communities in fragmented landscapes.

A conceptual model of movement ecology has recently been advanced to explain all movement by considering the interaction of four elements: internal state, motion capacity, navigation capacities, and external factors. We modified this framework to generate predictions for species richness dynamics of fragmented plant communities and tested them in experimental landscapes across a 7-year time series. We found that two external factors, dispersal vectors and habitat features, affected species colonization and recolonization in habitat fragments and their effects varied and depended on motion capacity. Bird-dispersed species richness showed connectivity effects that reached an asymptote over time, but no edge effects, whereas wind-dispersed species richness showed steadily accumulating edge and connectivity effects, with no indication of an asymptote. Unassisted species also showed increasing differences caused by connectivity over time, whereas edges had no effect. Our limited use of proxies for movement ecology (e.g., dispersal mode as a proxy for motion capacity) resulted in moderate predictive power for communities and, in some cases, highlighted the importance of a more complete understanding of movement ecology for predicting how landscape conservation actions affect plant community dynamics.

Evolutionary ecology of pungency in wild chilies.

The primary function of fruit is to attract animals that disperse viable seeds, but the nutritional rewards that attract beneficial consumers also attract consumers that kill seeds instead of dispersing them. Many of these unwanted consumers are microbes, and microbial defense is commonly invoked to explain the bitter, distasteful, occasionally toxic chemicals found in many ripe fruits. This explanation has been criticized, however, due to a lack of evidence that microbial consumers influence fruit chemistry in wild populations. In the present study, we use wild chilies to show that chemical defense of ripe fruit reflects variation in the risk of microbial attack. Capsaicinoids are the chemicals responsible for the well known pungency of chili fruits. Capsicum chacoense is naturally polymorphic for the production of capsaicinoids and displays geographic variation in the proportion of individual plants in a population that produce capsaicinoids. We show that this variation is directly linked to variation in the damage caused by a fungal pathogen of chili seeds. We find that Fusarium fungus is the primary cause of predispersal chili seed mortality, and we experimentally demonstrate that capsaicinoids protect chili seeds from Fusarium. Further, foraging by hemipteran insects facilitates the entry of Fusarium into fruits, and we show that variation in hemipteran foraging pressure among chili populations predicts the proportion of plants in a population producing capsaicinoids. These results suggest that the pungency in chilies may be an adaptive response to selection by a microbial pathogen, supporting the influence of microbial consumers on fruit chemistry.

Impacts of climate warming on terrestrial ectotherms across latitude.

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.